Membrane-induced step in the activation of Sendai virus fusion protein

Journal of Molecular Biology

Volumn 285, Issue 2, 1999, Pages 609-625

  Ben Efraim, Iris ^a   Kliger, Yossef ^a   Hermesh, Chen ^a   Shai, Yechiel ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Fluorescence; FTIR heptad repeat; Membrane fusion; Peptide membrane interactions

Indexed keywords

AMPHOLYTE; FLUORESCENT DYE; PEPTIDE; VIRUS FUSION PROTEIN;

ALPHA HELIX; AQUEOUS SOLUTION; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; FOURIER TRANSFORMATION; INFRARED SPECTROSCOPY; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; SENDAI VIRUS; VIRUS CELL INTERACTION;

RNA VIRUSES; SENDAI VIRUS;

EID: 0033555680     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2370     Document Type: Article

References (76)

1. 2(+)-ATPase protein of sarcoplasmic reticulum labeled with 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole. FEBS Letters. 259:1990;254-256.
2. Bartlett G. R. Phosphorus assay in column chromatography. J. Biol. Chem. 234:1959;466-468.
3. Bernstein H. B., Tucker S. P., Kar S. R., McPherson S. A., McPherson D. T., Dubay J. W., Lebowitz J., Compans R. W., Hunter E. Oligomerization of the hydrophobic heptad repeat of gp41. J. Virol. 69:1995;2745-2750.
4. Blacklow S. C., Lu M., Kim P. S. A trimeric subdomain of the simian immunodeficiency virus enveloped glycoprotein. Biochemistry. 34:1995;14955-14962.
5. Bosch M. L. Identification of the fusion peptide of primate immunodeficiency viruses. Science. 244:1989;694-696.
6. Buckland R., Malvoisin E., Beauverger P., Wild F. A leucine zipper structure present in the measles virus fusion protein is not required for its tetramerization but is essential for fusion. J. Gen. Virol. 73:1992;1703-1707.
7. Cameron D. G., Casal H. L., Gudgin E. F., Mantsch H. H. The gel phase of dipalmitoyl phosphatidylcholine. An infrared characterization of the acyl chain packing. Biochim. Biophys. Acta. 596:1980;463-467.
8. Carr C. M., Kim P. S. A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell. 73:1993;823-832.
9. Chambers P., Pringle C. R., Easton A. J. Sequence analysis of gene encoding the fusion glycoprotein of pneumonia virus of mice suggests possible conserved secondary structure elements in paramyxovirus fusion glycoproteins. J. Gen. Virol. 73:1992;1717-1724.
10. Chan D. C., Kim P. S. HIV entry and its inhibition. Cell. 93:1998;681-684.
11. Chan D. C., Fass D., Berger J. M., Kim P. S. Core structure of gp41 the HIV envelope protein. Cell. 89:1997;263-273.
12. Chen S. S., Lee S. F., Hao H. J., Chuang C. K. Mutations in the leucine zipper-like heptad repeat sequence of human immunodeficiency virus type 1 gp41 dominantly interfere with wild-type virus infectivity. J. Virol. 72:1998;4765-4774.
13. Chen S. S. L., Lee C. N., Lee W. R., McIntosh K., Lee T. H. Mutational analysis of the leucine zipper-like motif of the human immunodeficiency virus type 1 envelope transmembrane glycoprotein. J. Virol. 67:1993;3615-3619.
14. Chen Y. H., Yang J. T., Chau K. H. Determination of the helix and beta form of proteins in aqueous solution by circular dichroism. Biochemistry. 13:1974;3350-3359.
15. Doms R. W., Lamb R. A., Rose J. K., Helenius A. Folding and assembly of viral membrane proteins. Virology. 193:1993;545-562.
16. Dubay J. W., Roberts S. J., Brody B., Hunter E. Mutations in the leucine zipper of the human immunodeficiency virus type 1 transmembrane glycoprotein affect fusion and infectivity. J. Virol. 66:1992;4748-4756.
17. +-induced membrane insertion of influenza virus hemagglutinin involves the HA2 amino-terminal fusion peptide but not the coiled coil region. J. Biol. Chem. 271:1996;13417-13421.
18. Epand R. F., Martin I., Ruysschaert J. M., Epand R. M. Membrane orientation of the SIV fusion peptide determines its effect on bilayer stability and ability to promote membrane fusion. Biochem. Biophys. Res. Commun. 205:1994;1938-1943.
19. Fass D., Harrison S. C., Kim P. S. Retrovirus envelope domain at 1.7 Ångstrom resolution. Nature Struct. Biol. 3:1996;465-469.
20. Freed E. O., Myers D. J., Risser R. Characterization of the fusion domain of the human immunodeficiency virus type 1 envelope glycoprotein gp41. Proc. Natl Acad. Sci. USA. 87:1990;4650-4654.
21. Frey S., Tamm L. K. Membrane insertion and lateral diffusion of fluorescence-labelled cytochrome c oxidase subunit IV signal peptide in charged and uncharged phospholipid bilayers. Biochem. J. 272:1990;713-719.
22. Fringeli U. P., Günthard H. H. Infrared membrane spectroscopy. Grell E. Membrane Spectroscopy. 1981;270-332 Springer Verlag, Berlin and Heidelberg.
23. Fung B. K., Stryer L. Surface density determination in membranes by fluorescence energy transfer. Biochemistry. 17:1978;5241-5248.
24. Furuta R. A., Wild C. T., Weng Y., Weiss C. D. Capture of an early fusion-active conformation of HIV-1 gp41. Nature Struct. Biol. 5:1998;276-279.
25. Gazit E., Shai Y. Structural and functional characterization of the alpha 5 segment of Bacillus thuringiensis delta-endotoxin. Biochemistry. 32:1993;3429-3436.
26. Gazit E., Miller I. R., Biggin P. C., Sansom M. S. P., Shai Y. Structure and orientation of the mammalian antibacterial peptide cecropin P1 within phospholipid membranes. J. Mol. Biol. 258:1996;860-870.
27. Gething M. J., White J. M., Waterfield M. D. Purification of the fusion protein of Sendai virus: analysis of the NH2-terminal sequence generated during precursor activation. Proc. Natl Acad. Sci. USA. 75:1978;2737-2740.
28. Gething M. J., Doms R. W., York D., White J. Studies on the mechanism of membrane fusion: site-specific mutagenesis of the hemagglutinin of influenza virus. J. Cell Biol. 102:1986;11-23.
29. Ghosh J. K., Ovadia M., Shai Y. A leucine zipper motif in the ectodomain of Sendai virus fusion protein assembles in solution and in membranes and specifically binds biologically-active peptides and the virus. Biochemistry. 36:1997;15451-15462.
30. Ghosh J. K., Peisajovich S. G., Ovadia M., Shai Y. Structure-function study of a heptad repeat positioned near the transmembrane domain of Sendai virus fusion protein which blocks virus-cell fusion. J. Biol. Chem. 273:1998;27182-27190.
31. Greenfield N., Fasman G. D. Computed circular dichroism spectra for the evaluation of protein conformation. Biochemistry. 8:1969;4108-4116.
32. Harrick N. J. Internal Reflection Spectroscopy. 1967.
33. Haywood A. M. Characteristics of Sendai virus receptors in a model membrane. J. Mol. Biol. 83:1974;427-436.
34. Homma M., Ohuchi M. Trypsin action on the growth of Sendai virus in tissue culture cells. J. Virol. 12:1973;1457-1465.
35. Ishiguro R., Kimura N., Takahashi S. Orientation of fusion-active synthetic peptides in phospholipid bilayers: determination by Fourier transform infrared spectroscopy. Biochemistry. 32:1993;9792-9797.
36. Jackson M., Mantsch H. H. The use and misuse of FTIR spectroscopy in the determination of protein structure. Crit. Rev. Biochem. Mol. Biol. 30:1995;95-120.
37. Kliger Y., Shai Y. A leucine zipper-like sequence from the cytoplasmic tail of the HIV-1 envelope glycoprotein binds and perturbs lipid bilayers. Biochemistry. 36:1997;5157-5169.
38. Kliger Y., Aharoni A., Rapaport D., Jones P., Blumenthal R., Shai Y. Fusion peptides derived from the HIV type 1 glycoprotein 41 associate within phospholipid membranes and inhibit cell-cell fusion: structure-function study. J. Biol. Chem. 272:1997;13496-13505.
39. Lamb R. A. Paramyxovirus fusion: a hypothesis for changes. Virology. 197:1993;1-11.
40. Lambert D. M., Barney S., Lambert A. L., Guthrie K., Medinas R., Davis D. E., Bucy T., Erickson J., Merutka G., Petteway S. R. Peptides from conserved regions of paramyxovirus fusion (F) proteins are potent inhibitors of viral fusion. Proc. Natl Acad. Sci. USA. 93:1996;2186-2191.
41. Lawless M. K., Barney S., Guthrie K. I., Bucy T. B., Petteway S. R., Merutka G. HIV-1 membrane fusion mechanism: structural studies of the interactions between biologically-active peptides from gp41. Biochemistry. 35:1996;13697-13708.
42. Lear J. D., DeGrado W. F. Membrane binding and conformational properties of peptides representing the NH2 terminus of influenza HA-2. J. Biol. Chem. 262:1987;6500-6505.
43. Lelkes P. I. Liposome Technology. 1984;CRC Press, Boca Raton.
44. Loew L. M., Rosenberg I., Bridge M., Gitler C. Diffusion potential cascade. Conventional detection of transferable membrane pores. Biochemistry. 22:1983;837-844.
45. Loyter A., Volsky D. J. Reconstituted Sendai virus envelopes as carrier for the introduction of biological material into animal cells. Cell Surf. Rev. 8:1982;215-266.
46. Lu M., Blacklow S. C., Kim P. S. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nature Struct. Biol. 2:1995;1075-1082.
47. Malashkevich V. N., Chan D. C., Chutkowski C. T., Kim P. S. Crystal structure of the simian immunodeficiency virus (SIV) gp41 core: conserved helical interactions underlie the broad inhibitory activity of gp41 peptides. Proc. Natl Acad. Sci. USA. 95:1998;9134-9139.
48. Martin I., Schaal H., Scheid A., Ruysschaert J. M. Lipid membrane fusion induced by the human immunodeficiency virus type 1 gp41 N-terminal extremity is determined by its orientation in the lipid bilayer. J. Virol. 70:1996;298-304.
49. Matthews T. J., Wild C., Chen C. H., Bolognesi D. P., Greenberg M. L. Structural rearrangements in the transmembrane glycoprotein after receptor binding. Immun. Rev. 140:1994;93-104.
50. Mu ñ I., Durell S., Sakaguchi K., Appella E., Blumenthal R. Dilation of the human immunodeficiency virus-1 envelope glycoprotein fusion pore revealed by the inhibitory action of a synthetic peptide from gp41. J. Cell Biol. 140:1998;315-323.
51. Nieva J. L., Nir S., Muga A., Go ñ F. M., Wilschut J. Interaction of the HIV-1 fusion peptide with phospholipid vesicles: different structural requirements for fusion and leakage. Biochemistry. 33:1994;3201-3209.
52. Pereira F. B., Go ñ F. M., Nieva J. L. Liposome destabilization induced by the HIV-1 fusion peptide. Effect of a single amino acid substitution. FEBS Letters. 362:1995;243-246.
53. Pouny Y., Rapaport D., Mor A., Nicolas P., Shai Y. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry. 31:1992;12416-12423.
54. Rabenstein M., Shin Y. K. A peptide from the heptad repeat of human immunodeficiency virus gp41 shows both membrane binding and coiled coil formation. Biochemistry. 34:1995;13390-13397.
55. Rafalski M., Lear J. D., DeGrado W. F. Phospholipid interactions of synthetic peptides representing the N-terminus of HIV gp41. Biochemistry. 29:1990;7917-7922.
56. Rajarathnam K., Hochman J., Schindler M., Ferguson M. S. Synthesis, location, and lateral mobility of fluorescently labeled ubiquinone 10 in mitochondrial and artificial membranes. Biochemistry. 28:1989;3168-3176.
57. Rapaport D., Shai Y. Interaction of fluorescently labeled pardaxin and its analogues with lipid bilayers. J. Biol. Chem. 266:1991;23769-23775.
58. Rapaport D., Shai Y. Interaction of fluorescently labeled analogues of the amino-terminal fusion peptide of Sendai virus with phospholipid membranes. J. Biol. Chem. 269:1994;15124-15131.
59. Rapaport D., Ovadia M., Shai Y. A synthetic peptide corresponding to a conserved heptad repeat domain is a potent inhibitor of Sendai virus-cell fusion: an emerging similarity with functional domains of other viruses. EMBO J. 14:1995;5524-5531.
60. Rothschild K. J., Clark N. A. Anomalous amide I infrared absorption of purple membrane. Science. 204:1979;311-312.
61. Scheid A., Choppin P. W. Two disulfide-linked polypeptide chains constitute the active F protein of paramyxoviruses. Virology. 80:1977;54-60.
62. Sechoy O., Philippot J. R., Bienvenue A. F protein-F protein interaction within the Sendai virus identified by native bonding or chemical cross-linking. J. Biol. Chem. 262:1987;11519-11523.
63. Shai Y., Bach D., Yanovsky A. Channel formation properties of synthetic pardaxin and analogues. J. Biol. Chem. 265:1990;20202-20209.
64. Sims P. J., Waggoner A. S., Wang C. H., Hoffmann J. R. Studies on the mechanism by cyanine dyes measure membrane potential in red blood cells and phosphatidylcholine vesicles. Biochemistry. 13:1974;3315-3330.
65. Stegmann T., Doms R. W., Helenius A. Protein-mediated membrane fusion. Annu. Rev. Biophys. Biophys. Chem. 18:1989;187-211.
66. Strahilevitz J., Mor A., Nicolas P., Shai Y. Spectrum of antimicrobial activity and assembly of dermaseptin-b and its precursor form in phospholipid membranes. Biochemistry. 33:1994;10951-10960.
67. Tamm L. K., Tatulian S. A. Infrared spectroscopy of proteins and peptides in lipid bilayers. Quart. Rev. Biophys. 30:1997;365-429.
68. Vanini S., Longhi R., Lazzarin A., Vigo E., Siccardi A. G., Viale G. Discrete regions of HIV-1 gp41 defined by syncytia-inhibiting affinity purified human antibodies. AIDS. 7:1993;167-174.
69. Weissenhorn W., Dessen A., Harrison S. C., Skehel J. J., Wiley D. C. Atomic structure of the ectodomain from HIV-1 gp41. Nature. 387:1997;426-430.
70. Wild C., Oas T., McDanal C., Bolognesi D., Matthews T. A synthetic peptide inhibitor of human immunodeficiency virus replication: correlation between solution structure and viral inhibition. Proc. Natl Acad. Sci. USA. 89:1992;10537-10541.
71. Wild C. T., Shugars D. C., Greenwell T. K., McDanal C. B., Matthews T. J. Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 are potent inhibitors of virus infection. Proc. Natl Acad. Sci. USA. 91:1994a;9770-9774.
72. Wild C., Dubay J. W., Greenwell T., Baird T. J., Oas T. G., McDanal C., Hunter E., Matthews T. Propensity for a leucine zipper-like domain of human immunodeficiency virus type 1 gp41 to form oligomers correlates with a role in virus-induced fusion rather than assembly of the glycoprotein complex. Proc. Natl Acad. Sci. USA. 91:1994b;12676-12680.
73. Wild C., Greenwell T., Shugars D., Rimsky-Clarke L., Matthews T. The inhibitory activity of an HIV type 1 peptide correlates with its ability to interact with a leucine zipper structure. AIDS Res. Human Retrovir. 11:1995;323-325.
74. Wu C. S. C., Ikeda K., Yang J. T. Ordered conformation of polypeptides and proteins in acidic dodecyl sulfate solution. Biochemistry. 20:1981;566-570.
75. Yang P. W., Stewart L. C., Mantsch H. H. Polarized attenuated total reflectance spectra of oriented purple membranes. Biochem. Biophys. Res. Commun. 145:1987;298-302.
76. Yu Y. G., King D. S., Shin Y.-K. Insertion of a coiled-coil peptide from influenza virus hemagglutinin into membranes. Science. 266:1994;274-276.